The Terrestrial Isopod Microbiome: An All-in-One Toolbox for Animal–Microbe Interactions of Ecological Relevance

Abstract

Bacterial symbionts represent essential drivers of arthropod ecology and evolution, influencing host traits such as nutrition, reproduction, immunity, and speciation. However, the majority of work on arthropod microbiota has been conducted in insects and more studies in non-model species across different ecological niches will be needed to complete our understanding of host–microbiota interactions. In this review, we present terrestrial isopod crustaceans as an emerging model organism to investigate symbiotic associations with potential relevance to ecosystem functioning. Terrestrial isopods comprise a group of crustaceans that have evolved a terrestrial lifestyle and represent keystone species in terrestrial ecosystems, contributing to the decomposition of organic matter and regulating the microbial food web. Since their nutrition is based on plant detritus, it has long been suspected that bacterial symbionts located in the digestive tissues might play an important role in host nutrition via the provisioning of digestive enzymes, thereby enabling the utilization of recalcitrant food compounds (e.g., cellulose or lignins). If this were the case, then (i) the acquisition of these bacteria might have been an important evolutionary prerequisite for the colonization of land by isopods, and (ii) these bacterial symbionts would directly mediate the role of their hosts in ecosystem functioning. Several bacterial symbionts have indeed been discovered in the midgut caeca of terrestrial isopods and some of them might be specific to this group of animals (i.e., Candidatus Hepatoplasma crinochetorum, Candidatus Hepatincola porcellionum, and Rhabdochlamydia porcellionis), while others are well-known intracellular pathogens (Rickettsiella spp.) or reproductive parasites (Wolbachia sp.). Moreover, a recent investigation of the microbiota in Armadillidium vulgare has revealed that this species harbors a highly diverse bacterial community which varies between host populations, suggesting an important share of environmental microbes in the host-associated microbiota. In this review, we synthesize our current knowledge on the terrestrial isopod microbiome and identify future directions to (i) fully understand the functional roles of particular bacteria (both intracellular or intestinal symbionts and environmental gut passengers), and (ii) whether and how the host-associated microbiota could influence the performance of terrestrial isopods as keystone species in soil ecosystems.

The functional microbiome of arthropods

“…In particular, the functional groups of beta proteobacteria are not only similar to each other, but also statistically not dissimilar to group a of alpha and group b of alpha and gamma proteobacteria (Fig 4C), even if their visual comparison does shows some distinctive features (Fig 5B). Statistically significant levels of similarity between functional groups from different proteobacterial classes can be interpreted in terms of functional redundancy, a pattern previously found in diverse microbiomes [3,5,30,42,45]. Functional redundancy, together with the correspondence between functional groups and taxonomic clusters (for groups a, b and c in Fig 1, groups a and c in Fig 2 and group c in Fig 3), are consistent with the concept that environmental filtering could be the major driving force for structuring microbiomes [3,5,18,30].…”

“…Statistically significant levels of similarity between functional groups from different proteobacterial classes can be interpreted in terms of functional redundancy, a pattern previously found in diverse microbiomes [3,5,30,42,45]. Functional redundancy, together with the correspondence between functional groups and taxonomic clusters (for groups a, b and c in Fig 1, groups a and c in Fig 2 and group c in Fig 3), are consistent with the concept that environmental filtering could be the major driving force for structuring microbiomes [3,5,18,30]. To illustrate the functional redundancy across the taxonomic spectrum of bacterial microbiomes [3], the functional groups of all proteobacterial classes have been graphically compared from deep to late branching taxa along both orthogonal axes (Fig 5B).…”

Gut microbiomes of mobile predators vary with landscape context and species identity

“…We propose that food resource abundance and diversity in the local habitat could be one of the main drivers for both gut bacterial richness and host fat content. Further, diet‐related bacteria can potentially affect host fitness directly when they serve as a supplemental food source, temporarily contribute to digestion processes (Bouchon et al., ) or facilitate adaption to novel food sources (Chu, Spencer, Curzi, Zavala, & Seufferheld, ). However, if and to what extend a predator benefits from a mixed diet (Evans, Stevenson, & Richards, ; Harwood et al., ; Lefcheck, Whalen, Davenport, Stone, & Duffy, ; Lundgren, ) and diverse gut bacteria depends on host species: In our study, the two native beetles H. convergens and H. parenthesis had more body fat when their guts harbored many different bacterial.…”

“…Gut microbes can be vertically transmitted or acquired from the environment (horizontal transmission; Gibson & Hunter, ; Mason & Raffa, ). In addition, the total gut community also includes transient species that cannot permanently colonize the gut (Dillon, Vennard, Buckling, & Charnley, ; Erkosar & Leulier, ) but may represent a supplementary food source, or contribute to digestion (Bouchon, Zimmer, & Dittmer, ). Understanding factors influencing animal gut microbiome composition can thus yield important insights into ecological interactions.…”

Symbiosis-inspired approaches to antibiotic discovery

“…7 The insect gut, in particular, harbors a vast array of symbiotic microbial diversity and many studies have demonstrated the profound importance of these associations on insect digestive and immune systems. 8–12 Studies of these systems have been remarkably productive. Importantly, such studies with insects have curiously, served as a prelude to more recent efforts focused on human-microbe symbioses in which in vivo generated natural products play a clear role in human health.…”